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Biological Psychology 77 (2008) 353358


www.elsevier.com/locate/biopsycho

Anxiety impairs decision-making: Psychophysiological evidence


from an Iowa Gambling Task
Andrei C. Miu a,*, Renata M. Heilman a, Daniel Houser b,*
a
Program of Cognitive Neuroscience, Department of Psychology, Babes-Bolyai University, 37 Republicii, Cluj-Napoca, CJ 400015, Romania
b
Interdisciplinary Center for Economic Science and Department of Economics, George Mason University,
4400 University Drive, MSN 1B2, Fairfax, VA 22030, USA
Received 23 December 2006; accepted 30 November 2007
Available online 10 January 2008

Abstract
Using the Iowa Gambling Task (IGT) and psychophysiological correlates of emotional responses (i.e., heart rate and skin conductance), we
investigate the effects of trait anxiety (TA) on decision-making. We find that high TA is associated with both impaired decision-making and
increased anticipatory physiological (somatic) responses prior to advantageous trials. For both high and low TA, skin conductance responses
preceding advantageous trials predict decisions. At the same time, somatic responses to choice outcomes reflect differences between high and low
TA sensitivities to punishments and rewards. The pattern of impaired decision-making and increased somatic markers that we find in high TA may
have important implications for neuropsychological decision theory. In particular, it offers an example of defective modulation of somatic signals,
coupled with disrupted discrimination of advantageous and disadvantageous choices.
# 2008 Elsevier B.V. All rights reserved.

Keywords: Anxiety; Emotion and decision-making; Somatic markers

1. Introduction personality in decision-making. For instance, some timely


studies that approached the influence of personality on
It is by now widely accepted that emotion plays an adaptive decision-making found that sensation-seeking positively
role in human decision-making (for review see Bechara et al., correlated with the frequency of advantageous choices (Reavis
2000; Dunn et al., 2006). Discovering the physiological and Overman, 2001), whereas negative emotionality negatively
correlates and neurobiological underpinnings of emotions correlated with the frequency of choices from high-punishment
influence on decision, as well as the role individual differences decks (Peters and Slovic, 2000). These studies suggested
might play in this regard, is the ambitious goal of a rapidly personality differences, particularly those associated with
expanding literature (e.g., Kurzban and Houser, 2001; McCabe emotional reactivity such as TA, might provide a partial
et al., 2001; Decety et al., 2004). Here we contribute to this explanation for the high variance of IGT performance in
literature by reporting data from experiments using the Iowa healthy volunteers (Bechara and Damasio, 2005).
Gambling Task (IGT) that provide novel evidence on joint TA reflects individual differences in sensitivity to threat
relationships among trait anxiety (TA), somatic signaling and (Spielberger, 1966; Endler and Kocovski, 2001; Gray and
decision-making. McNaughton, 2000/2003, pp. 338). These individual differ-
IGT is a decision-making task simulating uncertainty of ences have been functionally translated into attentional,
premises and outcomes, as well as reward and punishment in memory, and interpretative biases towards the preferential
controlled laboratory conditions (Bechara et al., 1994). IGT has processing of aversive stimuli (e.g., Calvo et al., 2003). The
proven extremely valuable in studies of the effects of biological basis of this personality dimension has been
extensively studied from the genetic (Lau et al., 2006; Lesch
et al., 1996; Buckholtz et al., in press) to the neural systems
* Corresponding authors.
level (Grachev and Apkarian, 2000; Yamasue et al., 2008;
E-mail addresses: andrei_miu@emcoglab.org (A.C. Miu), Paulus et al., 2004). These studies indicated that TA is
dhouser@gmu.edu (D. Houser). considerably supported by additive genetic factors, some of
0301-0511/$ see front matter # 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.biopsycho.2007.11.010
354 A.C. Miu et al. / Biological Psychology 77 (2008) 353358

which are already known (e.g., variants of the serotonin age  standard deviation [S.D.]: 19.5  1 years) based on their >1 S.D. above or
below average scores on the trait portion of the Romanian version of Spielbergers
transporter and monoamine oxidase A genes), and it is
State-Trait Anxiety Inventory (STAI-X) (Spielberger, 1983; Pitariu et al., 1987),
associated with morphological, neurochemical and functional and the anxiety/neuroticism scale of the Romanian version of Zuckerman
brain differences in neural networks (e.g., prefrontal cortex, Kuhlman Personality Inventory (Zuckerman et al., 1993; Opre et al., 2003).
amygdala) that were previously related to emotion. The scores on these scales are reported in Table 1. The low TA group included 5
The relationship between TA and decision-making has women and 3 men, and the high TA group included 6 women and 2 men, with no
received attention only very recently. Using self-report significant socio-demographic (e.g., education, ethnic origin, native language)
differences between these groups. All the participants gave their informed consent
measures of risk perception and a decision-making task to participate to this experiment. The experimental procedures complied with the
explicitly involving risk evaluation, several studies found that recommendations of the Declaration of Helsinki and the national and institutional
TA was associated with increased avoidance of risky decision ethical guidelines for experiments with human participants.
and pessimistic risk appraisals (Maner et al., 2007; Maner and
Schmidt, 2006; Mitte, 2007). However, we are aware of no 2.2. Behavioral task
study investigating effects of TA on decision-making using
We used the standardized manual version of IGT, as described in Bechara
complex tasks such as IGT, which is thought to involve covert
et al. (1994). Briefly, participants were presented face downward four decks of
emotional signals that might adaptively guide decision-making cards labelled A, B, C, and D, with 40 cards in each deck. The participants
even before explicit knowledge about the task is available (see received a loan of 2000 Romanian New Currency (RON) facsimile at the
Bechara et al., 1997; and Maia and McClelland, 2004). beginning of the game and they were instructed to play the game so as to lose the
Considering that TA has been associated with preattentional least amount of money and win the most. The total number of trials was set at
100 card selections, without the participant being aware of how many cards he
cognitive biases (for review see Mathews and Mackintosh,
or she was going to pick. Turning each card from any deck carried an immediate
1998), investigating the effect of TA on decisions involving reward (100 RON for A and B, and 50 RON for C and D). However, A and B
emotional cues that preattentionally guide performance would were disadvantageous decks because every 10 cards from decks A and B over
be an important empirical contribution. the course of trials not only gain 1000 RON but also carried several unexpected
The present study investigates effects of TA on IGT penalties of 150350 RON (A) or a single large penalty (B) that raised the total
loss to 1250 RON. C and D were advantageous decks because they gained 500
performance, and obtains measures on the physiological
RON over 10 card selections and carried a total loss of 250 RON either
correlates of somatic signals that are expected to inform cumulated from several cards associated with 2575 RON penalties (C), or
decision-making (Bechara et al., 1997; Crone et al., 2004). We from only one 250 RON penalty card. Thus A and B were equivalent in terms of
design our study to provide evidence on two key related total loss over trials, and so were C and D in terms of total gain over trials. The
hypotheses. First, we hypothesize that high TA participants will difference was that while A and C had higher frequency but lower magnitude
punishments, B and D had lower frequency but higher magnitude punishments.
show lower IGT performance compared to low TA participants.
Playing mostly from the disadvantageous decks led to an overall loss, while
Second, we hypothesize that high TA participants will display this playing mostly from the advantageous decks led to an overall gain. The
lower performance concurrently with relatively high task-related performance of the participant was indexed by the CDAB score.
somatic signalling. We discuss below that these two hypotheses,
both of which our data support, are not necessarily inconsistent 2.3. Electrophysiological recordings
with the somatic marker hypothesis (Bechara et al., 2000). The
During IGT, we recorded electrocardiography (ECG) and skin conductance
reason is that the somatic marker hypothesis admits, under certain
(SCR) using a Biopac MP150 system (Biopac Systems, CA, USA). ECG was
conditions, uncoupling of somatic signals and ultimate decisions. recorded with a sample rate of 500 Hz, from three EL258RT Ag-AgCl electro-
des filled with isotonic GEL101 gel, positioned in a modified lead-2 placement.
2. Materials and methods SCRs were recorded via two TSD203 electrodermal response electrodes also
filled with isotonic gel and attached to the volar surfaces of the index and medius
2.1. Participants fingers. All the recordings were screened for physiological artifacts (e.g.,
motion) and analyzed offline using AcqKnowledge 3.5. The peak of the R-
Out of an initial cohort of 112 Babes-Bolyai undergraduate students who waves were used for the calculation of heart rate (HR) in beats per minute
agreed to be screened for this study, we selected 11 women and 9 men (mean (BPM) in each of the intervals of interest, from which we subtracted the value of an

Table 1
Scores on the trait portion of State-Trait Anxiety Inventory (STAI) and ZuckermanKuhlman Personality Inventory of participants included in this study
Category Women Men
TA low TA high TA low TA high
STAI-TA 27.66 W 0.57 58.83 W 4.26 26 W 3.74 57.5 W 4.94
ZKPQ anxiety/neuroticism 2 W 0.3 18 W 1.41 0.8 W 0.2 11
ZKPQ aggression/hostility 7.8  5.44 9.5  2.58 4.33  3.05 8.5  2.12
ZKPQ activity 12.2  2.58 8.33  3.82 13.33  1.15 6.5  4.94
ZKPQ sociability 8.2  7.1 8.5  5 9  3.6 5.5  6.36
ZKPQ sensation-seeking 9  4.18 11  3.74 9.33  1.15 10  1.41
Note: The data are reported as mean  standard deviation. No participant from this sample scored above 3 on the Infrequency scale of ZuckermanKuhlman
Personality Questionnaire (ZKPQ), which suggests either inattention to the content of the items and acquiescence or a very strong social desirability set (Zuckerman
et al., 1993). The unusually high standard deviations of scores other than TA and anxiety/neuroticism are justified by the specific selection of the participants for
opposing extreme scores of TA and anxiety/neuroticism (bold values).
A.C. Miu et al. / Biological Psychology 77 (2008) 353358 355

individual functional baseline estimated from recordings made during a relaxed


state before the experiment. We made sure that the HR functional baseline was not
contaminated by anticipatory stress mainly by simultaneously monitoring SCRs,
which are a reliable index of emotional arousal. From SCR recordings, we
extracted the area under the curve (mS/s) of SCRs in the intervals of interest,
after the downdrift in the SCR waves was eliminated using the difference
function of AcqKnowledge, as described in Bechara et al. (1999). It is noteworthy
that the effect of time differences between intervals of interest, particularly
anticipatory intervals (see below), was controlled by estimating SCRs per unit
of time. All the participants included in this study displayed SCRs during the IGT.
The intervals of interest were of two kinds, comprising (i) 5 s intervals after each
card was turned, which, depending on the type of the card, were of the reward or
punishment type; and (ii) anticipatory intervals between the end of each 5 s
reward or punishment interval and before the next card selection.

2.4. Data analyses

The behavioral and electrophysiological data were statistically processed


using analysis of variance (ANOVA) followed by Scheffe post hoc tests,
corrected for repeated measures as necessary. All analysis was conducted using
SPSS. The effect of sex on HR and SCR is supported by physiological
mechanisms independent of this task. Consequently, we focused on the main
effects of sex on behavioral performance, and the effects of TA  sex inter-
actions on physiological outcome measures.

3. Results

3.1. Behavior

A 2 (TA: high vs. low)  2 (sex: men vs. women) ANOVA of


CDAB scores indicates that TA (F[1,18] = 4.44, P < 0.05)
has a statistically significant effect on IGT performance
(Fig. 1A). High TA participants show decreased IGT
performance compared to low TA participants (Scheffe test:
mean difference = 5.09; criterion difference = 4.44, P < 0.05).
We find no statistically significant main effect of sex or
interaction of TA  sex on behavioral performance. Also,
neither TA nor the interaction of TA  sex is significantly
related to the time required to complete 100 trials in IGT
(mean  standard deviation: 11.00  1.09 min).
Fig. 1. Iowa Gambling Task performance (A), anticipatory skin conductance
3.2. Anticipatory somatic responses responses (SCRs) (B) and heart rate (HR) (C) in high and low trait anxiety (TA)
participants. *P < 0.01.
The analyses of anticipatory HR and SCRs indicated that
before making a selection, participants generally displayed
cardiac deceleration and higher SCRs. The amplitude of We investigated whether anticipatory effects developed
anticipatory SCRs was generally higher for disadvantageous during the task by analyzing the effect of TA on physiological
compared to advantageous trials (F[1,18] = 4.5, P < 0.05). measures in advantageous trials for each block of 20 trials. The
However, only anticipatory SCRs in advantageous trials effect of TA on anticipatory HR reached statistical significance
predicted the CDAB scores in IGT (r2 = 0.087, P < 0.008). in the second block of trials (F[1,18] = 4.17, P < 0.04), and its
We obtain significant effects of TA on physiological measures magnitude increased until the last block (F[1,18] = 19.23,
made before advantageous trials, high TA being associated with P < 0.0001). Similarly, the effect of TA on anticipatory SCRs
increased physiological responses in anticipation of advanta- was marginally significant by the end of the first block of trials
geous trials. In contrast, TA had non-significant effects on (F[1,18] = 3.29, P < 0.07), and its magnitude increased until
anticipatory HR and SCRs in disadvantageous trials. Specifi- the last block (F[1,18] = 10.29, P < 0.004).
cally, in comparison to low TA participants, high TA participants
displayed increased cardiac deceleration (F[1,18] = 16.04, 3.3. Somatic responses to outcomes
P < 0.0001) and SCR amplitude (F[1,18] = 7.07, P < 0.008)
before advantageous trials. Our data also reveal a significant The analyses of physiological responses to reward and
interaction of TA  sex on anticipatory HR deceleration and punishment indicate that HR is sensitive to the emotional
SCRs in advantageous trials (P < 0.05). valence of the behavioral outcome, with higher cardiac
356 A.C. Miu et al. / Biological Psychology 77 (2008) 353358

deceleration in the trials associated with punishment (mean Reekum, 2005), allowing that some emotions may have
difference = 4.96) than in those associated with rewards (mean detrimental consequences to decision outcomes. To the extent
difference = 2.95). Moreover, the analyses of physiological this is true, it might be possible to improve decision-making
measures as a function of trial (advantageous vs. disadvanta- through psychological and even pharmacological interventions
geous) and outcome (reward vs. punishment) indicate several (e.g., beta blockers to reduce anxiety interference in high TA).
significant differences associated with TA. High TA partici- Finally, it is known that TA correlates with neural activity in
pants display higher cardiac deceleration in advantageous trials structures including the amygdala, specifically when emotional
associated with punishment than those associated with rewards stimuli are preattentionally processed (Etkin et al., 2004). IGT
(F[1,18] = 4.55, P < 0.05). There is also a statistically also probably relies on preattentionally processed emotional
significant interaction of TA  sex on punishment HR in cues. Consequently, we speculate that high TA may be
advantageous trials (P < 0.01). Low TA participants show associated with distinct patterns of neural activation triggered
higher reward SCRs compared to punishment SCRs in both by secondary inducers of somatic signals (i.e., entities
advantageous (F[1,18] = 10.32, P < 0.001) and disadvanta- generated by the recall of a personal or hypothetical emotional
geous trials (F[1,18] = 12.74, P < 0.0004). Low TA partici- event; see Bechara et al., 2000) in structures such as the
pants also display higher HR in disadvantageous trials amygdala and ventromedial prefrontal cortex. If so, IGT
associated with rewards compared to those associated with decisions could be affected.
punishment (F[1,18] = 7.51, P < 0.006). The effect of TA on IGT performance is also informed by a
previous interesting study by Peters and Slovic (2000) who
report an inverse relationship between negative emotionality
4. Discussion
and choices from high-punishment decks. This is particularly
noteworthy in light of the theoretical and empirical work that
This study yields two main findings consistent with our
connects TA and behavioral inhibition measures (see, e.g., Gray
predictions. We find that high TA is associated with impaired
and McNaughton, 2000/2003 for the former; and Carver and
decision-making in IGT, and that this is apparently uncoupled
White, 1994; Zinbarg and Mohlman, 1998, for the latter). The
from the increased and potentially adaptive anticipatory
present studys results are potentially reconciled with Peters
somatic signals in high TA.
and Slovic (2000) by noting that we selected extreme TA
There are at least four mechanisms that might explain the
participants for our study, while the median split approach was
association between high TA and impaired decision-making.
used by Peters and Slovic (2000) as well as in other recent
One is related to the previously demonstrated relationship
studies of TA and decision (Maner et al., 2007; Maner and
between anxiety and the tendency to use fewer cues and
Schmidt, 2006; Mitte, 2007). The implication is that it would be
inefficiently select relevant from irrelevant cues in reasoning
useful to conduct additional research to determine whether the
tasks (Leon and Revelle, 1985). Indeed, high TA participants
effects we identify are robust to those with less extreme TA.
may have attended to a more limited set of data, with the
In our study high TA was not only associated with impaired
blinders caused by their high anxiety (see also the third
IGT performance but also with increased anticipatory
mechanism described below) making them focus mostly on the
physiological responses prior to advantageous trials. Moreover,
easily understood rewards, which are the same for every choice
these physiological responses were evidently acquired during
from a given deck. This could have led them to choose from the
the task since the magnitude of this effect developed over trials.
high-reward disadvantageous decks more often.1
This set of results is important for at least three reasons. First, it
A second possible mechanism relates to the tendency of
seems to support the importance of somatic markers to
increased declarative elaboration on choices, which has been
decision-making by indicating that advantageous trials were
associated with high TA (e.g., Calvo et al., 2003). This tendency
preceded by increased HR deceleration, a psychophysiological
would be counterproductive in a complex decision-making task
index of orientation (see, e.g., Bradley, 2000), and an increase
like IGT in which declarative cues on the optimum gambling
in SCR amplitude. Moreover, anticipatory SCRs in advanta-
strategy typically become available between trials 50 and 80 in
geous choices predicted IGT performance. However, since we
healthy volunteers (Bechara et al., 1997).
did not control the level of declarative knowledge in the task in
A third mechanism potentially underlying the positive
this study, these results cannot exclude the involvement of
association between impaired decisions and high TA could
declarative knowledge in IGT performance (Maia and McClel-
involve distraction by emotions unrelated to the task, which is
land, 2004).
more likely to occur in high TA participants (Spielberger, 1966;
Second, at least for high TA, these results seem to provide an
Endler and Kocovski, 2001). One such emotion is anticipatory
example of uncoupling between decision-making performance
stress, which has been previously shown to impair IGT
and somatic markers. This is in line with a previous suggestion
performance (Preston et al., 2007), and to which high TA
that some healthy volunteers may override the adaptive
participants may be predisposed. This is consistent with the
influence of their somatic markers by higher cognitive
idea that emotion is not one thing (Davidson and van
processes (Bechara et al., 2000). Indeed, this is consistent
with the pattern of high autonomic reactivity (e.g., Gonzalez-
1
We acknowledge the suggestion made by one of the reviewers in regard to Bono et al., 2002; Zahn et al., 1991; Cornwell et al., 2006) and
this mechanism. increased tendency to declaratively elaborate on emotional
A.C. Miu et al. / Biological Psychology 77 (2008) 353358 357

stimuli (Calvo et al., 2003), which has been previously Bolla, K.I., Eldreth, D.A., Matochik, J.A., Cadet, J.L., 2004. Sex-related
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Crone et al., 2004) in which cardiovascular measures of somatic L.G., Berntson, G.G. (Eds.), Handbook of Psychophysiology. second ed.
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